Insufficient nutrient intake in individuals with disabling hearing loss and the restoration of nutritional sufficiency in hearing aid users

Hearing loss affects some nutrient intake. Disabling hearing loss may exacerbate these issues. We aimed to evaluate nutrient intake and assess deficiencies based on functional hearing status. The study included 6907 participants with information on demographic factors, nutrient intake, weight, height, disease status, and hearing level in the eighth Korea National Health and Nutrition Examination Survey, conducted from 2019 to 2021. We categorized the participants into 3 groups based on their functional hearing status: bilateral hearing, unilateral hearing, and disabling hearing loss. The disabling hearing loss group showed lower intake of most major nutrients (P < 0.05), dietary fiber (P < 0.001), and most minerals and vitamins (P < 0.05), with some insufficiencies. The unilateral hearing group showed lower intake only for potassium (P = 0.036) compared to the bilateral hearing group and significantly higher intake of hydration (P = 0.039), dietary fiber (P = 0.039), and calcium (P = 0.009) than the disabling hearing loss group. Nutrient insufficiency in the disabling hearing loss group was more prominent in women, and was partially resolved by using hearing aids. Clinicians and nutritionists should consider undernourishment in these patients, and appropriate interventions for nutrition and hearing aids should be recommended.


Subjects and data extraction
We extracted data on participants in the eighth Korea National Health and Nutrition Examination Survey (KNHANES), which was conducted from 2019 to 2021.The survey comprised 22,559 participants.These participants were selected using two-stage stratification and random sampling methods to prevent selection bias.Of these, 9795 individuals who had undergone pure tone audiometry were selected.Audiometry was performed exclusively on individuals over 40 years old in the eighth KNHANES, considering the prevalence of hearing loss, which sharply increases with age, particularly in individuals aged over 40 31 .Therefore, only middle-aged and older adults were included in our study.Subsequently, we narrowed down the cohort to those with normal tympanic membranes and complete data on gender, age, economic status, education level, height, weight, nutritional intake, and medical history, specifically regarding hypertension, dyslipidemia, stroke, coronary artery disease, diabetes mellitus, major depressive disorder, otitis media, chronic kidney disease, gout, and liver cirrhosis.The information on nutritional intake was collected by the investigators, who visited households and evaluated food intake based on participants' recall for the 24 h preceding the survey.Ultimately, 6907 participants met the criteria and were included in this study (Fig. 1).All methods used in the eighth KNHANES survey and our study were carried out in accordance with the relevant guidelines and regulations, and our study was conducted based on the STROBE statement.The eighth KNHANES survey was conducted after obtaining informed consent from all participants and receiving approval from the Institutional Review Board (IRB No. 2018-01-03-C-A, 2018-01-03-2C-A, 2018-01-03-5C-A).

Classification of the participants according to their hearing status
Disabling hearing loss is characterized by a hearing loss greater than 40 dB in the better ear.The term "functional hearing" refers to a hearing level below 40 dB, differentiating it from disabling hearing loss.Participants were categorized into three groups according to their functional hearing status: the bilateral hearing group, which had bilateral hearing levels below 40 dB; the unilateral hearing group, which had functional hearing in one ear and more than moderate hearing loss (> 40dB) in the other; and the disabling hearing loss group, which had a bilateral hearing loss exceeding 40 dB.

Nutritional status evaluation
We utilized the KDRI as the benchmark for determining insufficient intake of each nutrient.The KDRI provides guidelines for the estimated average requirement (EAR), recommended dietary allowance (RDA), and adequate intake (AI).We assessed the insufficiency of nutrient intake against these references.

Subgroup analysis of differences in nutrient intake based on the use of hearing aids
Since hearing loss patients typically use hearing aids when their hearing level is around 50 dB, and patients with hearing thresholds below 50 dB usually exhibit a tendency to refuse the use of hearing aids, 32,33 we selected patients with hearing loss greater than 50 dB.Subsequently, we included patients with information about hearing aid use, excluding the three patients who had undergone cochlear implantation (Fig. 1).

Statistical analysis
Analysis of variance and the chi-square test were utilized to compare demographic and socioeconomic factors, as well as the prevalence of medical history, across the study groups.Following this, multivariate analysis of covariance (MANCOVA) was conducted to determine the adjusted average and standard error, taking into account variables such as gender, age, weight, height, and medical history.The MANCOVA calculations were also carried out separately for male and female participants.The adjusted mean and standard error for each group, along with the KDRI values, were subsequently normalized by dividing them by the adjusted mean value for the total cohort.This normalization process was designed to evaluate nutritional insufficiency by creating a ratio that reflects the average intake relative to that of the entire study population.All statistical analyses were performed using IBM SPSS Statistics 25.0 (IBM Corp., Armonk, N.Y., USA).

Nutritional intake differences among the groups
In an age-and gender-adjusted analysis, significant differences were observed among the groups in their intake of energy, hydration, protein, polyunsaturated fatty acids, omega-3 fatty acids, omega-6 fatty acids, cholesterol, carbohydrates, total dietary fiber (TDF), sugar, calcium, phosphate, potassium, magnesium, iron, zinc, vitamin A, vitamin D, vitamin E, carotene, thiamine, riboflavin, niacin, folate, and vitamin C. The results of the post-hoc tests are presented in Fig. 2.
After adjusting for age, gender, household income, educational status, height, weight, hypertension, dyslipidemia, stroke, coronary artery disease, diabetes mellitus, and previous history of otitis media, significant differences were observed in the intake of energy, hydration, protein, carbohydrates, TDF, sugar, calcium, phosphate, potassium, magnesium, iron, vitamin A, vitamin D, vitamin E, beta-carotene, thiamine, riboflavin, niacin, folate, and vitamin C among the groups.Post-hoc analysis revealed that all nutrient intake levels that differed significantly between groups were lower in the disabling hearing loss group compared to the bilateral hearing loss group.The unilateral hearing loss group had lower potassium intake than the bilateral hearing loss group.Additionally, the unilateral hearing loss group had significantly higher intake of hydration, TDF, and calcium compared to the disabling hearing loss group, as shown in Fig. 3A.

Differences in nutrient intake among the groups of male participants
A subgroup analysis was conducted for the male population.After adjusting for other factors, we observed differences in nutrient intake between the groups, which included hydration, carbohydrates, TDF, calcium, and potassium.The intake levels of all these nutrients were greater in the bilateral hearing group compared to the disabling hearing loss group except for potassium.No differences in nutrient intake were noted between the bilateral and unilateral hearing groups (Fig. 3B).

Differences in nutrient intake among the groups of female participants
In female participants, the consumption of energy, hydration, protein, omega-3 fatty acids, TDF, sugar, calcium, phosphate, potassium, magnesium, iron, zinc, vitamin E, carotene, thiamine, riboflavin, niacin, folate, and vitamin C differed significantly among the groups after adjusting for other factors.In the post-hoc analysis, the bilateral hearing group showed higher nutrient intake compared to the disabling hearing loss group, with the   exception of energy.The intake of hydration, omega-3 fatty acids, magnesium, iron, zinc, thiamine, and folate was also notably lower in the disabling hearing loss group compared to the unilateral hearing group.No significant differences were observed in nutrient intake between the bilateral and unilateral hearing groups (Fig. 3C).

Male participants
The calcium, vitamin A, and vitamin C intake of all groups of male participants did not meet the EAR (Fig. 3B).Additionally, all groups showed insufficient intake of magnesium, niacin, and folate based on the RDI (Fig. 3B).Moreover, the intake of hydration, potassium, vitamin D, and vitamin E was lower than the AI in all groups.The TDF intake was lower than the AI in the unilateral hearing group and the disabling hearing loss group (Fig. 3B).

Female participants
All groups of female participants showed insufficient intake of energy, calcium, vitamin A, niacin, folate, and vitamin C based on the EAR.Additionally, the disabling hearing loss group exhibited insufficient thiamine intake based on this criterion (Fig. 3C).Potassium and thiamine intake was also lower than the RDI values in all groups.Furthermore, the disabling hearing loss group showed deficient magnesium, iron, zinc, and riboflavin intake based on the RDI (Fig. 3C).Additionally, hydration, vitamin D, and vitamin E intake did not meet the AI in all groups (Fig. 3C).

Differences in nutrient intake based on the use of hearing aids
There were 57 hearing aid users and 121 non-hearing aid users (Fig. 1).Among the analyzed factors-namely, age, gender, household income, education level, weight, height, medical history, and bilateral mean hearing level calculated by averaging the pure tone audiometry at 0.5 kHz, 1 kHz, 2 kHz, and 4 kHz-the educational level (P = 0.012) and mean hearing level (P = 0.001) exhibited statistically significant differences between the hearing aid users and non-users.

Discussion
Hearing loss is associated with a range of functions and health conditions, including physical and mental health, nutritional intake, and economic status [4][5][6]8,9,21,22,[34][35][36][37] . We categorized ndividuals by their functional hearing status to assess differences in nutritional intake across these groups.Our findings showed that varied aspects of nutritional intake were correlated with the degree of disabling hearing loss.Specifically, the quantity of nutrient consumption decreased progressively with worsening functional hearing status in middle-aged and older adults, even after adjusting for other variables.Nutrient intake levels, including hydration, protein, carbohydrates, TDF, sugar, calcium, phosphate, potassium, magnesium, iron, vitamin A, vitamin D, vitamin E, the vitamin B complex, and vitamin C, were notably lower in the group with disabling hearing loss compared to those with bilateral hearing, as determined by multivariable analysis.Furthermore, nutritional deficiencies were more pronounced among women with disabling hearing loss.The group with unilateral hearing loss had higher consumption of some nutrients compared to those with disabling hearing loss and exhibited certain differences from the bilateral hearing group in age-and gender-adjusted analysis.However, these differences in nutrient intake were not statistically significant in the unilateral hearing group relative to the bilateral hearing group after adjusting for additional factors.
Moreover, the intake of hydration, calcium, potassium, magnesium, vitamin A, vitamin D, vitamin E, niacin, folate, and vitamin C did not meet the KDRI in all male groups.Additionally, the TDF intake was below the KDRI recommendations for both the unilateral hearing loss group and the disabling hearing loss group.Female participants also demonstrated inadequate intakes of energy, hydration, calcium, vitamin A, vitamin D, vitamin E, thiamine, niacin, folate, and vitamin C according to the KDRI.Moreover, women with disabling hearing loss had insufficient intake of magnesium, iron, zinc, thiamine, and riboflavin, according to the KDRI guidelines.The prevalence of nutrient insufficiency was significantly higher in the groups with disabling hearing loss for both men and women.Consequently, individuals in the disabling hearing loss group were at an increased risk of nutritional deficiencies, including hydration, energy, and various essential minerals and vitamins.
There were no significant differences in the intake of most nutrients between the bilateral hearing group and the unilateral hearing group upon multivariable analysis.Potassium, which did show variations between the two groups, was found to be consumed in lower level than AI by both.The other nutrient deficiencies observed in the unilateral hearing group, compared to the bilateral functional group, were for TDF and calcium, according to the KDRI.Nonetheless, the differences in intake levels between the bilateral and unilateral hearing groups were not statistically significant.Consequently, the unilateral hearing group demonstrated a slightly insufficient nutrient status, akin to that of the bilateral hearing group.The reason for the less meaningful association between unilateral hearing and nutritional intake is the slight degree of functional loss in the unilateral hearing group.Although individuals with unilateral functional hearing may experience some functional loss compared to those with normal hearing, these issues are not as profound as those encountered by individuals with disabling www.nature.com/scientificreports/hearing loss 23,25 .In contrast, the disabling hearing loss group exhibited significant differences in the intake of many nutrients, with some levels falling below the recommended thresholds.Energy deficiency can induce low lean mass 38 .Inadequate hydration has been linked to metabolic impairment, degenerative diseases, decreased kidney function, impaired skin barrier function, and cognitive impairment 39 .Since calcium is a key factor for osteogenesis, calcium metabolism, and preventing osteoporosis, sufficient calcium intake is necessary for middle-aged and older adults 40 .Additionally, calcium deficiency has been associated with age-related diseases such as atherosclerosis, neurodegenerative diseases, degenerative arthritis, and malignancy 40 .Magnesium is the second most common intracellular cation, and it is essential for energy production and nucleic acid synthesis 41 .It has also been linked to various symptoms and diseases, including asthma, osteoporosis, migraine, metabolic syndrome, and muscle cramps 41 .Iron plays a pivotal role in hematopoiesis and is important in preventing anemia 42 .Zinc is crucial for growth and reproduction,30 and is necessary for numerous physiological processes.Deficiency in zinc can lead to dermatitis, impaired growth, and an increased risk of infection 41 .Vitamin A is important for eye function and the immune system [43][44][45][46] .Deficiency in vitamin A can manifest as eye signs such as night blindness, conjunctival xerosis, corneal xerosis, and eye ulcers 44,46 .Vitamin D is very important for preventing rickets, osteoporosis, and neurodegenerative diseases [47][48][49] .Vitamin E acts as an antioxidant, scavenging reactive oxygen species, and plays a role in immunomodulation 50 .Its deficiency has been linked to infections and growth problems 51 .The vitamin B complex is associated with megaloblastic anemia, physical function, and central nervous system functions, including cognitive decline, depression, confusion, epileptiform convulsions, and Wernicke-Korsakoff syndrome in cases of severe thiamine deficiency 52 .www.nature.com/scientificreports/Additionally, vitamin C serves as an antioxidant and as a cofactor for certain enzymes, such as hydroxylase, which is necessary for collagen synthesis 53 .Recent studies have suggested that vitamin C may have a role in the prevention or treatment of some infections 54 .Furthermore, a severe deficiency of vitamin C can result in scurvy 53 .These essential and significant nutrients were found to be more deficient in participants with disabling hearing loss than in either of the other two groups.This deficiency could lead to a higher prevalence of physical and mental problems.Moreover, research by Le Prell et al., has shown that intake of magnesium and vitamins A, E, and C can prevent noise-induced hearing loss by neutralizing free radicals, as demonstrated in animal studies.Additionally, several prospective and randomized controlled studies have indicated that consumption of omega-3 fatty acids, magnesium, and vitamins A, E, B, and C may help prevent hearing loss [13][14][15][16][17][18] .Consequently, nutrient insufficiency in patients with hearing loss can exacerbate the condition and negatively impact overall health.Therefore, nutritional interventions, including supplements or dietary consultations, should be considered essential for those with disabling hearing loss to prevent further hearing loss as well as other health complications.Such measures could play a crucial role in preserving both the physical and mental well-being of these patients.
Nutrient insufficiency can also occur in association with other diseases.A previous study examining the nutritional status of individuals with depression found that these patients often have deficiencies in protein and energy, as well as lower intakes of folate and vitamin B12, when compared to recommended dietary allowances 55 .Similarly, research by Weikel et al. indicated that patients with cataracts commonly exhibit deficiencies in vitamins B and C, lutein/zeaxanthin, omega-3 fatty acids, multivitamins, and carbohydrates, relative to recommended nutrient levels 56 .Similarly, our research found that patients with disabling hearing loss were at risk of inadequate nutrient intake.Investigating the impact of various disorders on nutritional status is crucial to prevent additional complications arising from the primary diseases.
Differences in nutrient intake among the groups were observed in the consumption of some major nutrients, some fatty acids, various vitamins, and minerals.Conversely, no differences were noted in the intake of fat, saturated fatty acids (SFA), cholesterol, and sodium.Generally, fat, SFA, cholesterol, and sodium are considered unhealthy nutrients.These findings align with a previous study by Choi et al. 22 , which reported that fruit consumption in the bilateral hearing loss group was lower than that in the normal hearing group.In addition, our results are consistent with previous studies that have reported associations between omega-3 fatty acids, minerals, or vitamins and hearing loss 8,9,21,22 .Therefore, individuals with disabling hearing loss seem to consume fewer healthy foods and a greater proportion of unhealthy foods compared to those with bilateral functional hearing.This pattern of nutrient intake should be considered when developing dietary interventions.
In this study, insufficient nutrient intake among the female population appeared to be more closely linked to disabling hearing loss.Kushwaha et al. 57 reported that women were more prone to malnutrition.Schilp et al. 58 also demonstrated a significant association between the female gender and malnutrition.Additionally, women tend to be more susceptible to functional loss associated with hearing loss 7,20 .Previous studies have reported that female hearing loss patients experienced higher levels of depression and loneliness than male hearing loss patients 7,20 .Our results are consistent with these tendencies.Therefore, nutritional interventions should be particularly targeted toward female patients with disabling hearing loss.
Compared to previous studies on the association between hearing loss and nutrient intake 8,9 , we classified individuals as having disabling hearing loss or functional hearing.Since disabling hearing loss critically affects other functions 23,25,59 , the differences in nutrient intake among the groups might be more prominent in our study than in previously conducted studies.
Additionally, the use of hearing aids proved helpful in compensating for nutritional insufficiency in individuals with bilateral disabling hearing loss, exceeding 50 dB.Given that hearing aids can mitigate some adverse consequences of hearing loss, including enhancing social network status and alleviating depressive symptoms 6,35,36 , they may influence nutritional status.Additional research is needed to elucidate the effect of hearing aids on nutrient intake.
The participants in this survey were selected using two-stage stratification and random-sampling methods to prevent selection bias.However, despite the short-term recall periods before the survey, as the data on nutritional intake were collected through participant recall, the potential for recall errors existed.Prospective nutritional data collection would be helpful in preventing these kinds of errors in future studies.
Since this study employed a cross-sectional design, it was not possible to evaluate the causality between disabling hearing loss and nutrient intake.Emmett et al. 37 found that malnutrition during childhood can impact the hearing levels in young adults.Because nutrient deficiency can induce hearing loss, a prospective cohort study could be instrumental in demonstrating the causality of this association.
Another limitation of our study is the lack of information on other audiological exams, such as bone conduction hearing levels or speech audiometry.Since the KNHANES did not include other audiological examinations, we could not evaluate the association of other audiological results with nutritional intake.A further study, including speech audiometry, may be helpful for assessing the relationship between daily speech recognition ability and nutrient intake.

Conclusion
Individuals with disabling hearing loss are susceptible toseveral significant nutrient deficiencies, and this tendency was more pronounced in women.Given the possibility of undernourishment in patients with disabling hearing loss, hearing aid use and appropriate nutritional interventions, including nutritional consultation or supplementation, could enhance the physical and mental health of this patient population.

Figure 1 .
Figure 1.A flow chart of subject selection for the analysis of the association between hearing loss and nutritional intake (depicted in red) and between hearing aid usage and nutritional intake (depicted in blue).KNHANES, Korea National Health and Nutrition Examination Survey; N, number of participants; CI, cochlear implant.

Table 1 .
Demographic factors, socioeconomic factors, height, weight, and medical history of each group.Significant values are in [bold].